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Contents Summary 27 I. Introduction 28 II. Developmental constraint or a phyletic legacy? 29 III. Green plant phylogeny 29 IV. The ancestral green plant life cycle 31 V. Haplobiontic or diplobiontic life cycles? 32 VI. Pseudo-archegonia, plasmodesmata, and parenchyma 33 VII. Genomic re-deployment and embryophyte reproduction 35 VIII. Developmental homologies? 35 IX. Isomorphic or dimorphic? 36 X. Conclusions 38 Acknowledgements 39 References 39 Summary The extant land plants are unique among the monophyletic clade of photosynthetic eukaryotes, which consists of the green algae (chlorophytes), the charophycean algae (charophytes), numerous groups of unicellular algae (prasinophytes) and the embryophytes, by possessing, firstly, a sexual life cycle characterized by an alternation between a haploid, gametophytic and a diploid, sporophytic multicellular generation; secondly, the formation of egg cells within multicellular structures called archegonia; and, thirdly, the retention of the zygote and diploid sporophyte embryo within the archegonium. We review the developmental, paleobotanical and molecular evidence indicating that: the embryophytes descended from a charophyte-like ancestor; this common ancestor had a life cycle with only a haploid multicellular generation; and the most ancient (c. 410 Myr old) land plants (e.g. Cooksonia, Rhynia and Zosterophyllum) had a dimorphic life cycle (i.e. their haploid and diploid generations were morphologically different). On the basis of these findings, we suggest that the multicellular reproductive structures of extant charophytes and embryophytes are developmentally homologous, and that those of the embryophytes evolved by virtue of the co-option and re-deployment of ancient algal homeodomain gene networks.

The pyrimidine exchange type of RNA editing in land plant (embryophyte) organelles has largely remained an enigma with respect to its biochemical mechanisms, the underlying specificities, and its raison d'etre. Apparently arising with the earliest embryophytes, RNA editing is conspicuously absent in one clade of liverworts, the complex thalloid Marchantiidae. Several lines of evidence suggest that the large gene family of organelle-targeted RNA-binding pentatricopeptide repeat (PPR) proteins plays a fundamental role in the sequence-specific editing of organelle transcripts. We here describe the identification of PPR protein genes with plant-specific carboxyterminal (C-terminal) sequence signatures (E, E+, and DYW domains) in ferns, lycopodiophytes, mosses, hornworts, and jungermanniid liverworts, one subclass of the basal most clade of embryophytes, on DNA and cDNA level. In contrast, we were unable to identify these genes in a wide sampling of marchantiid liverworts (including the phylogenetic basal genus Blasia)--taxa for which no RNA editing is observed in the organelle transcripts. On the other hand, we found significant diversity of this type of PPR proteins also in Haplomitrium, a genus with an extremely high rate of RNA editing and a phylogenetic placement basal to all other liverworts. Although the presence of modularly extended PPR proteins correlates well with organelle RNA editing, the now apparent complete loss of an entire gene family from one clade of embryophytes, the marchantiid liverworts, remains puzzling.

† Background and Aims Consensus higher-level molecular phylogenies present a compelling case that an ancient divergence separates eukaryotic green algae into two major monophyletic lineages, Chlorophyta and Streptophyta, and a residuum of green algae, which have been referred to prasinophytes or micromonadophytes. Nuclear DNA content estimates have been published for less than 1% of the described green algal members of Chlorophyta, which includes multicellular green marine algae and freshwater flagellates (e.g. Chlamydomonas and Volvox). The present investigation summarizes the state of our knowledge and adds substantially to our database of C-values, especially for the streptophyte charophycean lineage which is the sister group of the land plants. A recent list of 2C nuclear DNA contents for isolates and species of green algae is expanded by 72 to 157. † Methods The DNA-localizing fluorochrome DAPI (4 0 ,6-diamidino-2-phenylindole) and red blood cell (chicken erythrocytes) standard were used to estimate 2C values with static microspectrophotometry. † Key Results In Chlorophyta, including Chlorophyceae, Prasinophyceae, Trebouxiophyceae and Ulvophyceae, 2C DNA estimates range from 0.01 to 5.8 pg. Nuclear DNA content variation trends are noted and discussed for specific problematic taxon pairs, including Ulotrichales‐Ulvales, and Cladophorales‐Siphonocladales. For Streptophyta, 2C nuclear DNA contents range from 0. 2t o 6.4 pg, excluding the highly polyploid Charales and Desmidiales, which have genome sizes of up to 14.8 and 46.8 pg, respectively. Nuclear DNA content data for Streptophyta superimposed on a contemporary molecular phylogeny indicate that early diverging lineages, including some members of Chlorokybales, Coleochaetales and Klebsormidiales, have genomes as small as 0.1‐0.5 pg. It is proposed that the streptophyte ancestral nuclear genome common to both the charophyte and the embryophyte lineages can be characterized as 1C ¼ 0.2 pg and 1n ¼ 6. † Conclusions These data will help pre-screen candidate species for the on-going construction of bacterial artificial chromosome nuclear genome libraries for land plant ancestors. Data for the prasinophyte Mesostigma are of particular interest as this alga reportedly most closely resembles the ‘ancestral green flagellate’. Both mechanistic and ecological processes are discussed that could have produced the observed C-value increase of .100-fold in the charophyte green algae whereas the ancestral genome was conserved in the embryophytes.

Land plants underwent tremendous evolutionary change following the divergence of the ancestral lineage from algal relatives. Several important developmental innovations appeared as the embryophyte clade diversified, leading to the appearance of new organs and tissue types. To understand how these changes came about, we need to identify the fundamental genetic developmental programs that are responsible for growth, patterning, and differentiation and describe how these programs were modified and elaborated through time to produce novel morphologies. Class III homeodomain–leucine zipper (class III HD–Zip) genes, identified in the model plant Arabidopsis thaliana, provide good candidates for basic land plant patterning genes. We show that these genes may have evolved in a common ancestor of land plants and their algal sister group and that the gene family has diversified as land plant lineages have diversified. Phylogenetic analysis, expression data from nonflowering lineages, and evidence from Arabidopsis and other flowering plants indicate that class III HD–Zip genes acquired new functions in sporophyte apical growth, vascular patterning and differentiation, and leaf development. Modification of expression patterns that accompanied diversification of class III HD–Zip genes likely played an important role in the evolution of land plant form.

Publisher Summary This chapter examines the differences in physiology among embryophytes and their algal ancestors, with particular emphasis on their water relations. The embryophytes have very significant variations in water relations and the chapter considers their evolution within the embryophytes as well as the evolution of embryophyte water relations from those of their algal ancestors. The chapter also examines the relationship of the likely evolution of embryophyte water relations to cladistic analyses of embryophyte phylogeny and to the fossil record. The physiological changes that occurred in the evolution from algal ancestors to the different grades of organization of embryophytes has been determined from the physiology of extant plants in relation to their phylogeny as determined by cladistic analysis and from the order in which anatomical features appeared in the fossil record. The fossil record of embryophytes also reveals certain characteristics of organisms that are not found today. The fossil record is not helpful in providing some information such as desiccation tolerance or intolerance, except by applying an empirical correlation from extant plants that no embryophyte more than 1 meter in height is desiccation tolerant in the vegetative phase. Overall, lines of evidence indicate that the earliest embryophytes were desiccation tolerant and poikilohydric.

Publisher Summary This chapter explores the current understanding of the origin of the spore wall, the function(s) of the spore wall in early land plants, and mode of spore wall formation in early land plants. The embryophytes are one of the major kingdoms of eukaryotice life. The sporopollenin wall surrounding charophycean zygotes and embryophyte spores/pollen grains is homologous, and the spore/pollen wall is an embryophyte synapomorphy that evolved as an adaptive response to the invasion of the land. It is considered that the primary function of the spore/pollen wall involves protection in the harsh subaerial environment. Regarding spore wall development, ultrastructural studies have demonstrated that structural elements present in the spore walls of extant plants can be recognized in the fossil spores of early land plants, suggesting that spore wall development was similar in extant and ancient land plants. Studies of molecular genetics of spore wall formation are in their infancy but have the potential to solve many unanswered questions regarding spore wall homologies and developmental processes—particularly when such studies are commenced on more “primitive” land plants and their extant sister group.

The earliest fossil evidence for land plants comes from microscopic dispersed spores. These microfossils are abundant and widely distributed in sediments, and the earliest generally accepted reports are from rocks of mid-Ordovician age (Llanvirn, 475 million years ago). Although distribution, morphology and ultrastructure of the spores indicate that they are derived from terrestrial plants, possibly early relatives of the bryophytes, this interpretation remains controversial as there is little in the way of direct evidence for the parent plants. An additional complicating factor is that there is a significant hiatus between the appearance of the first dispersed spores and fossils of relatively complete land plants (megafossils): spores predate the earliest megafossils (Late Silurian, 425 million year ago) by some 50 million years. Here we report the description of spore-containing plant fragments from Ordovician rocks of Oman. These fossils provide direct evidence for the nature of the spore-producing plants. They confirm that the earliest spores developed in large numbers within sporangia, providing strong evidence that they are the fossilized remains of bona fide land plants. Furthermore, analysis of spore wall ultrastructure supports liverwort affinities.

The embryophytes (land plants) have long been thought to be related to the green algal group Charophyta, though the nature of this relationship and the origin of the land plants have remained unresolved. A four-gene phylogenetic analysis was conducted to investigate these relationships. This analysis supports the hypothesis that the land plants are placed phylogenetically within the Charophyta, identifies the Charales (stoneworts) as the closest living relatives of plants, and shows the Coleochaetales as sister to this Charales/land plant assemblage. The results also support the unicellular flagellate Mesostigma as the earliest branch of the charophyte lineage. These findings provide insight into the nature of the ancestor of plants, and have broad implications for understanding the transition from aquatic green algae to terrestrial plants.

Dispersed microfossils (spores and phytodebris) provide the earliest evidence for land plants. They are first reported from the Llanvirn (Mid–Ordovician). More or less identical assemblages occur from the Llanvirn (Mid–Ordovician) to the late Llandovery (Early Silurian), suggesting a period of relative stasis some 40 Myr in duration. Various lines of evidence suggest that these early dispersed microfossils derive from parent plants that were bryophyte–like if not in fact bryophytes. In the late Llandovery (late Early Silurian) there was a major change in the nature of dispersed spore assemblages as the separated products of dyads (hilate monads) and tetrads (trilete spores) became relatively abundant. The inception of trilete spores probably represents the appearance of vascular plants or their immediate progenitors. A little later in time, in the Wenlock (early Late Silurian), the earliest unequivocal land plant megafossils occur. They are represented by rhyniophytoids. It is only from the Late Silurian onwards that the microfossil / megafossil record can be integrated and utilized in interpretation of the flora. Dispersed microfossils are preserved in vast numbers, in a variety of environments, and have a reasonable spatial and temporal fossil record. The fossil record of plant megafossils by comparison is poor and biased, with only a dozen or so known pre–Devonian assemblages. In this paper, the early land plant microfossil record, and its interpretation, are reviewed. New discoveries, novel techniques and fresh lines of inquiry are outlined and discussed.

Previously, a database characterizing examples of Embryophyte gene family lineages showing evidence of positive selection was reported. Of the gene family trees, 138 Embryophyte branches showed Ka/Ks>>1 and are candidates for functional adaptation. The database and these examples have now been studied in further detail to better understand the molecular basis for plant genome evolution. Neutral modeling showed an excess of positive and/or negative selection in the database over a neutral expectation centered on the mean Ka/Ks ratio. Out of 673 families with assigned structures, 490 have at least one branch with Ka/Ks >>1 in a region of the protein, enabling a picture of selective pressures delineated by protein structure. Most gene families allowed reconstruction back to the last common ancestor of flowering plants (Magnoliophytes) without saturation of 4- fold degenerate codon position. Positive selection occurred in a wide variety of gene families with different functions, including in the self incompatibility locus, in defense against pathogens, in embryogenesis, in cold acclimation, and in electrontransport. Structurally, selective pressures were similar between alpha-helices and beta- sheets, but were less negative and more variant on the surface and away from the hydrophobic core. Positive selection was detected statistically significantly in a small and nonrandom minority of gene families in a systematic analysis of embryophyte gene families. More sensitive methods increased the level of positive selection that was detected and presented a structural basis for the role of positive selection in plant genomes.

EVIDENCE for terrestrial vegetation in Ordovician and Silurian times, before the advent of vascular plants, comes from palyno-morphs (cryptospores1), that is, non-dissociating tetrads and dyads2,3 and cuticles4. The lack of a megafossil record for the spore producers is usually attributed to low fossilization potential of vegetative tissues, and this, plus spore type5, contributes to the hypothesis that the plants were embryophytes/archegoniates at a bryophyte level of organization3,5,6 and perhaps most similar in organization to modern hepatics5. Here we describe a minute coal-ified fossil from the Lower Devonian (Lochkovian: micrornatus-newportensis Spore Biozone) of the Welsh Borderland7, which contains obligate, smooth-walled tetrahedral tetrads, similar (by scanning electron microscopy) to those first recorded in the Ordovician. To our knowledge, these are the first data on the gross morphology and tissues of the plants that comprised the earliest embryophyte land flora (Gray's Eoembryophytic epoch3), albeit obtained from a relict Devonian example fossilized at a time when the composition of dispersed spore and megafossil assemblages suggests that tracheophytes and tracheophyte-like plants (rhyniophytoids) had generally begun to dominate land vegetation (Gray's Eotracheophyta3). Its anatomy in toto finds no exact parallels in embryophytes, but many of the individual cellular features match those in extant hepatics (liverworts).

The transition of plant life from aquatic algae to land plants was one of the major events in the history of life. However, in hypothesizing the evolutionary path of the transition, limited shared phenotypic characters in aquatic algae and land plants (embryophytes) have been a major hinderance. Chloroplast genomes contain characters useful in tracing evolutionary histories. Embryophyte chloroplast genomes are distinguished from algal cpDNAs by the presence of over 20 group II introns and three ribosomal protein operons (rpl23, clpP and 3Œrps12 operons). These phylogenomic features indicate a phylogenetic relationship of charophytes and embryophytes. In addition to these operons and introns, the evolution of rRNA and psbB operon evolution of streptophyte lineages will be incorporated with major biological phenotypic features to produce a phylogenetic tree. Basal embryophytes, the antithetic hypothesis, monophyly of embryophytes, and paraphyly of charophytes will be discussed. Strepotophytes are classified into three major groups (basal streptophytes, mid-divergent streptophytes and late divergent charophytes-embryophytes).

Macerations of Middle Ordovician (Llanvirnian) shales from Saudi Arabia yield an assemblage of spores of probable land plants (cryptospores), acritarchs, and chitinozoa. The production of sporopollenin-containing, sporelike tetrads is considered a fundamental character of the embryophytes, because no extant algae produce spores of this type. No trilete spores were found at this horizon, reinforcing previous assertions that obligate meiotic tetrads predate the earliest trilete spores. Sporomorph tetrads and dyads, in conjunction with cuticlelike fragments, were probably derived from terrestrial plants at a bryophyte grade. Although there are reports of possibly older cryptospores, the Hanadir assemblage described herein clearly establishes their presence by Llanvirnian time.

Considerable progress has been made recently, based on classical morphological characters and newly described ultrastructural features, in understanding the phylogenetic relationships of the tracheophytes to the green algae and bryophytes. Recent technological advances in molecular biology, particularly the advent of the polymerase chain reaction (PCR), have allowed nucleotide sequence data relevant to such large-scale phylogenetic questions to accumulate, especially ribosomal RNA gene sequences (both the large and small subunits) from the nucleus and the chloroplast. We present synthetic cladistic analyses of the green plants that combine and compare available morphological and molecular data sets

The colonization of land by streptophyte algae, ancestors of embryophyte plants, was a fundamental event in the history of life on earth. Bryophytes are early diversifying land plants that mark the transition from freshwater to terrestrial ecosystems. The amphibious liverwort Riccia fluitans can thrive in aquatic and terrestrial environments and thus represents an ideal organism to investigate this major transition. Therefore, we aimed to establish a transformation protocol for R. fluitans to make it amenable for genetic analyses. An Agrobacterium transformation procedure using R. fluitans callus tissue allows to generate stably transformed plants within 10 weeks. Furthermore, for comprehensive studies spanning all life stages, we demonstrate that the switch from vegetative to reproductive development can be induced by both flooding and poor nutrient availability. Interestingly, a single R. fluitans plant can consecutively adapt to different growth environments and forms distinctive and reversible features of the thallus, photosynthetically active tissue that is thus functionally similar to leaves of vascular plants. The morphological plasticity affecting vegetative growth, air pore formation, and rhizoid development realized by one genotype in response to two different environments makes R. fluitans ideal to study the adaptive molecular mechanisms enabling the colonialization of land by aquatic plants.

Background The terrestrial habitat was colonized by the ancestors of modern land plants about 500 to 470 million years ago. Today it is widely accepted that land plants (embryophytes) evolved from streptophyte algae, also referred to as charophycean algae. The streptophyte algae are a paraphyletic group of green algae, ranging from unicellular flagellates to morphologically complex forms such as the stoneworts (Charales). For a better understanding of the evolution of land plants, it is of prime importance to identify the streptophyte algae that are the sister-group to the embryophytes. The Charales, the Coleochaetales or more recently the Zygnematales have been considered to be the sister group of the embryophytes However, despite many years of phylogenetic studies, this question has not been resolved and remains controversial. Results Here, we use a large data set of nuclear-encoded genes (129 proteins) from 40 green plant taxa (Viridiplantae) including 21 embryophytes and six streptophyte algae, representing all major streptophyte algal lineages, to investigate the phylogenetic relationships of streptophyte algae and embryophytes. Our phylogenetic analyses indicate that either the Zygnematales or a clade consisting of the Zygnematales and the Coleochaetales are the sister group to embryophytes. Conclusions Our analyses support the notion that the Charales are not the closest living relatives of embryophytes. Instead, the Zygnematales or a clade consisting of Zygnematales and Coleochaetales are most likely the sister group of embryophytes. Although this result is in agreement with a previously published phylogenetic study of chloroplast genomes, additional data are needed to confirm this conclusion. A Zygnematales/embryophyte sister group relationship has important implications for early land plant evolution. If substantiated, it should allow us to address important questions regarding the primary adaptations of viridiplants during the conquest of land. Clearly, the biology of the Zygnematales will receive renewed interest in the future.

The importance of a cladistic approach in reconstructing the phylogeny of bryophytes is discussed and illustrated by an analysis of the major groups of bryophytes with respect to the tracheophytes and the green algae. The cladistic analysis, using 51 characters taken from the literature, gives the following tentative results: (1) the embryophytes as a whole are monophyletic; (2) the bryophytes (sensu lato) are paraphyletic; (3) the mosses share a more recent common ancestor with the tracheophytes than do the liverworts or hornworts; (4) the hornworts appear to share a more recent common ancestor with the moss-tracheophyte lineage than with the liverworts; however, the existence of several homoplasies makes this placement more problematical; (5) the origin of alternation of generations in the embryophytes, based on out-group comparison with their oogamous, haplontic, algal sister groups, was by progressive elaboration of the primitively epiphytic sporophyte generation; and (6) the presence of vascular tissue (xylem and phloem) can best be interpreted as a synapomorphy of the moss-tracheophyte clade, and tracheids (xylem with ornamented walls) as a synapomorphy of the tracheophytes; therefore, the prevailing designation of “vascular plants” for the tracheophytes alone is inaccurate.